Factors associated with adherence to oral HIV pre-exposure prophylaxis among female sex workers in the Mara Region, Tanzania: A 2022 cross-sectional study

Female sex workers (FSWs) have a higher risk of acquiring human immunodeficiency virus (HIV) infection compared with the general female population. Tanzania adopted pre-exposure prophylaxis (PrEP) use for HIV-negative key populations in 2019 as a strategy to reduce HIV transmission. We aimed to identify factors associated with PrEP adherence among FSWs in Tanzania. We conducted a cross-sectional study of FSWs using oral HIV PrEP from June-July 2022 in 5 Mara Region districts. Stata software was used to analyze the quantitative data. Poor overall PrEP adherence was observed among FSWs, with adherence of 48.3% (174/360) and 43.3% (156/360) according to pill count and self-reports, respectively. Participants living with family members had 2.32 higher odds of PrEP adherence (adjusted odds ratio [aOR] = 2.32, 95% confidence interval [CI] = 1.27–42.23, P = .006) versus participants living alone or with friends. Moreover, FSWs who preferred pill packages had 1.41 higher odds of adherence (aOR = 2.43, [95% CI = 1.41–4.19, P = .001]); participants with a good perception of PrEP had 1.71 higher odds (aOR = 1.71, [95% CI = 1.01–2.91, P = .047]) of PrEP adherence. We found that living with family, pill packaging, and PrEP perception played significant roles in PrEP adherence among FSWs. Interventions to improve pill packaging, social support, and the perception of PrEP among FSWs should be intensified to increase adherence in this vulnerable population.


Introduction
Human immunodeficiency virus (HIV) infection is a global public health concern and a significant cause of death, especially in developing countries. [1,2]Sub-Saharan Africa is the most severely affected region globally, accounting for nearly two-thirds of the global HIV burden.Biological, social, cultural, behavioral, economic, and structural variables contribute to this high burden. [3]stimates show that Tanzania has 1.9 million people living with HIV, of whom 77,000 contracted the disease initially and 24,000 died from acquired immunodeficiency syndrome (AIDS)-related illnesses in 2019. [1]The United Nations Program on HIV/AIDS (UNAIDs) reported that the rate of new infections in Tanzania was slowly decreasing. [4]The overall HIV prevalence among adults aged 15 to 49 years decreased with time, from 7% in 2003/2004 to 5.1% in 2011/2012 and 4.7% in 2016/2017. [5]Studies conducted among key populations in selected regions of Tanzania reported a prevalence of 28% among female sex workers (FSWs). [6]Owing to economic insecurity, inability to negotiate regular condom use, being assaulted, criminalization, and marginalization, sex workers are 14 times more likely to contract HIV than the general female population. [7]Therefore, FSWs play a crucial role in the transmission of HIV. [8]he World Health Organization (WHO) recommends the adoption of a number of combined preventive strategies, including anti-retroviral therapy usage among HIV-negative key populations, to reduce the number of new HIV infections. [9]This strategy is generally referred to as pre-exposure prophylaxis (PrEP), and is advised by the UNAIDS and WHO for groups with an annual risk of HIV acquisition > 3%. [10,11]vidence demonstrates that PrEP is highly effective and virtually eliminates the risk of contracting HIV through sexual intercourse by 99% when used consistently and correctly. [12]anzania adopted the use of PrEP between 2018 and 2019 to protect FSWs. [13][16][17] Literature on adherence to HIV oral PrEP is limited.This study aims to determine adherence and factors associated with non-adherence to oral HIV PrEP by gathering information related to the extent to which FSWs receive the PrEP service in the Mara region.

Ethical considerations
This study was approved by the Catholic University of Health and Allied Sciences and the National Health Research Ethics Subcommittee of the National Institute for Medical Research.Participation was voluntary, and written consent was obtained from the Participants.The participants retained the right to withdraw from the study at any time.

Study design and setting
This cross-sectional study was conducted among FSWs in selected health facilities in the Mara Region that offered PrEP services.Five councils, namely the Tarime District Council, Tarime Town Council, Rorya District Council, Musoma Municipal Council, and Bunda Town Council, were included in the study.The Mara Region is a focus area of the National AIDS Control Programme.Through the National AIDS Control Programme, FSWs receive PrEP at clinics in accordance with the Tanzania Ministry of Health with the aim of reducing HIV transmission.

Study participants
The sample size was estimated using the Kish-Leslie formula (1965) as follows: [19] Sample Size where N = minimum sample size; Z = confidence interval (CI) level at 95% (CI = 1.96);P is the proportion of PrEP adherence among FSWs based on a previous study conducted in Kampala, Uganda 71% [18] ; and d = 5% margin of error (standard value = 0.05).The sample size was calculated as follows: The minimum calculated sample size was 317.After adding 10% of the non-respondents the sample size was calculated as follows: 10/100 × 317 = 31.7 31.7 + 317 = 348.9 (3) Therefore, the sample size required to determine the level of adherence to the study was 349 FSWs taking oral HIV PrEP.

Sampling
Simple random sampling was used to select the 5 of 9 districts to be included in the study.These districts have many gold mining sites and numerous recreational sites, such as clubs, bars, hotels, pubs, massage parlors, and guesthouses, where FSWs work.To select the study participants, a simple random sampling method was used to select the health facilities that offered PrEP services for inclusion in the study, and interviews guided by community health workers familiar to the participants were conducted at the workplace.FSWs taking PrEP were proportionately divided among the selected health facilities, and a convenient sampling method was used to obtain eligible FSWs until the sample size was reached.In addition, every FSW who attended a clinic for PrEP refills or received PrEP service at the community outreach center and met the selection criteria were asked to participate in the study.

Variable and measure
The dependent variable was adherence, which was assessed using both self-reporting and pill count methods.The self-reporting method was used to measure adherence using 4 adherence questions, which were designed to measure adherence in a resource-constrained setting. [20]In order to maximize the precision of adherence measurement, the pill count method was also deployed to measure adherence.Key and vulnerable population client cards were used to verify the number of pills dispensed during the last visit, and adherence was calculated using the following formula [21] : % of adherence = 100 − % of missing pills (5)   Therefore, participants with > 95% pill use were considered to have good adherence.
The Independent variables were the number of clients per day, PrEP duration, pill color, pill package, pill refill site, education level, marital status, age, condom use, and risk level (7 questions were asked and risk was categorized by the scores).A score of 0 was regarded as no risk, 1 to 2 as low risk, 3 to 4 as moderate risk, and 5 to 7 as high risk.

Data collection
A structured questionnaire guided by the conceptual framework, which was developed from the social-ecological model, was used to collect data.Well-trained research assistants (healthcare workers, such as nurses) collected the data.
A structured questionnaire guided by the conceptual framework was used to determine the level of adherence and explore the factors associated with oral HIV PrEP among FSWs.
Participants were recruited when refilling their prescriptions at their respective health facilities and community outreach centers.This process was facilitated by the existing healthcare workers throughout the study period.Moreover, community outreach workers helped identify eligible participants for inclusion in the study.

Data analysis
Stata software (StataCorp LLC, College Station, TX) was used for data analysis.Categorical variables are described as proportions or percentages.Numerical variables are presented as means and medians with their corresponding standard deviations.
Multiple logistic regression analysis was performed to examine the association between the independent variables and adherence.The crude association of each independent variable was determined to examine its relationship with the dependent variable (adherence) in univariate models.Any variable with a P-value < 0.10 in the univariate test was considered a candidate for the multivariable model along with the variables of known clinical importance.Once the variables were identified, they were entered into the multivariate model.Associations are presented as odds ratios with 95% CIs.
We used the Hosmer-Lemeshow test to examine whether the final model adequately fitted the data for the multiple logistic regression model.An interaction test was performed to examine the effects of heterogeneity.The final parsimonious model (i.e., the model with significant findings for predictors) is presented.The model-building procedure and guidelines for reporting the regression analysis are described in detail elsewhere.

Sociodemographic characteristics of study participants
A total of 360 FSWs taking PrEP were enrolled in this study from June to July 2022.More than half of the participants (299/360, 83.1%) were Christians; 65% were older than 25 years; and the mean age was 28 ± 7 years.Most participants (225/360, 62.5%) were single, and almost half (179/360, 49.7%) had attained a primary level of education.Approximately one-third of participants (121/360, 33.6%) reported sex work as their main source of income.Among the 239 FSWs who reported that they had other jobs besides sex work, the majority (149/360, 62.3%) worked as bartenders.Details of the results are presented in Table 1.

HIV acquisition risk assessment among FSWs in mara region
The results showed that 54.2% (195/360) of participants had been working as a sex worker for more than 3 years.More than half of the participants (258/360, 71.7%) began engaging in commercial sex work when they were ≥ 18 years old, and approximately a quarter of FSWs (103/360, 28.6%) claimed to have at least 3 sex clients per day; 84.7% (305/360) used condoms for HIV prevention, although 80% (288/360) reported inconsistent condom use.Regarding HIV risk assessment, a relatively large number of participants (245/360, 68.1%) had moderate risk (Table 2).3).

PrEP adherence assessment
Generally, PrEP adherence was poor among participants in this study, with only 48.3% (174/360) and 43.3% (156/360) of participants adhering according to pill count and self-reporting, respectively.The agreement measure between the pill count and self-report methods was moderate, with kappa statistics of 0.44 (P < 0001) (Fig. 1).

Factors associated with good adherence to oral HIV PrEP among FSWs
In the multivariable analysis, living with family members adjusted odd ratio (aOR = 2.32, [95% CI = 1.27-4.23;P = .006])was an independent predictor of good adherence; participants living with family members were twice as likely to adhere to PrEP than participants living alone.The second predictor of good adherence was pills packaging.Participants who reportedly loved the current pill packaging had 2.43 higher odds of PrEP adherence (aOR = 2.43, [95% CI = 1.41-4.19;P = .001])compared with participants who disliked the pill packaging.The final predictor of good adherence was perception; participants who had a good perception of PrEP had 1.01 higher odds of PrEP adherence (aOR = 1.71 [95% CI = 1.01-2.91;P = .047])compared with participants with a poor perception of PrEP (Table 5).The remaining factors examined as independent predictors of adherence showed no significant effects.

Discussion
To reduce the number of new HIV infections, the WHO recommends the use of several prevention interventions combined, including ARV, among HIV-negative individuals with a substantial risk of HIV infection.This primary preventive approach is known as PrEP.Evidence shows that when taken consistently and correctly, PrEP is very effective and reduces the risk of HIV infection to near zero.The present study focused on identifying the factors associated with adherence to PrEP among FSWs.Our study found that the overall PrEP adherence among FSWs was 48.3%, which was lower than that observed in other countries. [18,22]The present study found that living with family, pill packaging, and perception of PrEP were associated with adherence.
This study provides evidence that living arrangements, such as living with family, are associated with good adherence to PrEP.The findings indicate that when a sex worker is a member of a family and the family depends on her self-prevention of acquiring HIV, she can continue to provide for her family through sex work.This further indicates that families can provide adherence support to participants.Our study findings were similar to those reported by Gombe et al [23] and Jackson-Gibson et al, [3] which showed that living arrangements positively improved adherence to PrEP.Our results indicate that when FSWs disclose their work to a family member, they show enhanced adherence to HIV prevention strategies.Hence, strengthening the disclosure of sex work as a source of income to families should be emphasized during PrEP education in this population.
Our data provides evidence that pill packaging is associated with good adherence among this population.This finding indicates that packaging, including colors, may influence adherence to PrEP.This finding is similar to that reported in another study by Gombe et al, [21] which showed that pill packaging is important for improving adherence to PrEP medication.Our findings indicate that pill packaging should be enhanced to promote adherence to PrEP and other related medications.
This study further demonstrated that a good perception of PrEP was associated with good adherence, indicating that sex workers with a good perception of PrEP adhered to PrEP.According to the PrEP implementation framework, all vulnerable people receive education and are assessed for eligibility before initiating this medication.Thus, sex workers who are well educated before receiving PrEP should have a positive perception, which enhances their adherence.Our findings are similar to those of another study conducted in Zimbabwe by Gombe et al, [22] which showed that good adherence was associated with the perception of the medication given.We recommend strengthening appropriate information on PrEP among sex workers to enhance adherence in this population.

Limitation
This study adopted a cross-sectional study design without a control group; thus, further studies are needed to show the temporal relationship.Moreover, our cross-sectional design did not include sex workers lost to follow-up.Because these sex workers were more likely to have experienced poor adherence, the results were biased toward better adherence by (naturally) excluding them.

Figure 1 .
Figure 1.Result of pre-exposure prophylaxis adherence according to self-report and pill count.

Table 4
Factors that hindered PrEP adherence among FSWs in June 2022.

Table 5
Bivariate and multivariate analysis of factors associated with adherence of oral HIV pre-exposure prophylaxis.Medicine3.3.PrEP characteristics and preferences of FSWsAll participants reported being counseled and screened for HIV infection and undergoing other baseline examinations before PrEP initiation.During the study period, all participants (360/360, 100%) received PrEP, although the duration of PrEP use varied.